The Role of Cross-Cue Reactivity in Coexisting Smoking and Gambling Habits

Edelgard Wulfert

Kristen Harris

James Broussard

University at Albany, Albany, NY, USA

This article was peer reviewed. All URLs were available at the time of submission.
For correspondence: Edelgard Wulfert, PhD, University at Albany, Department of Psychology, 1400 Washington
Ave., Albany, , NY 12222., e-mail: ewulfert@albany.eduEthics approval: This study, ‘Cue Reactivity in Gamblers, Smokers, and Smoking Gamblers,’ was approved by the Office of Regulatory
& Research Compliance (ORRC), University at Albany/SUNY.Competing interests: None declared.Acknowledgements: No external funding supported this research. The University at Albany/SUNY provided stipends to the doctoral
students involved in the research.

Abstract

Cigarette smoking is the most common addictive behaviour co-occurring with problem gambling. Based on classical conditioning,
smoking and gambling cues may acquire conditioned stimulus properties that elicit cravings for both behaviours. This study
examined cross-cue reactivity in 75 men who were regular smokers, poker players or cigarette-smoking poker players. Participants
were exposed to discrete cigarette, poker and neutral cues while skin conductance and psychological urges to smoke and gamble
were measured. Results showed evidence of cross-cue reactivity based on skin conductance, and subjective response to smoking
cues; subjective response to gambling cues was less clear. Smoking gamblers showed greater skin conductance reactivity to
cues, and stronger subjective urges to smoke to smoking and gambling cues, compared to individuals who only smoked or only
gambled. This study demonstrates evidence for cross-cue reactivity between a substance and a behavioural addiction, and the
results encourage further research.

The development and maintenance of addictive behaviours such as smoking and gambling have been explained via operant and classical
conditioning. Unconditioned physiological reactions (e.g., increased adrenaline output; heart rate arousal) and their psychological
correlates (the “high” feeling; the excitement of winning money) come to function as positive reinforcement and increase the
future probability of these behaviours. Through their association with reinforcement, previously neutral exteroceptive (i.e.,
discrete external or contextual stimuli) and interoceptive stimuli develop a cueing function and begin to elicit specific
psychological and physiological conditioned responses (Bouton, 2000). In a research setting, the conditioned reactions at the physiological level are often measured as changes in heart rate
or in skin conductance, and at the psychological level, as urges or craving to engage in the addictive behaviour. This phenomenon
has been termed cue reactivity (Drummond, 2001) and has been reliably shown with substances including cigarettes, alcohol, cocaine and heroin (for a meta-analysis, see
Carter & Tiffany, 1999). Cue reactivity is also a well-established phenomenon with recreational and pathological gamblers,
both in the laboratory (e.g., Blanchard, Wulfert, Freidenberg, & Malta, 2000; Sodano & Wulfert, 2010) and a real-world environment (e.g., Kushner et al., 2007).

The principles of operant and classical conditioning can also elucidate the co-occurrence of specific addictive behaviours.
For example, the high comorbidity between alcohol and tobacco dependence has been explained via cross-substance cue reactivity
(Zacny, 1990). Through the repeated use of cigarettes and alcohol together, one substance comes to act as a conditioned stimulus for the
other substance and elicits cravings for the immediate as well as the associated substance. This situation has been found
in nicotine and alcohol dependent individuals who experienced urges to smoke when exposed to alcohol cues, and vice versa
(e.g., Burton & Tiffany, 1997; Drobes, 2002; Traylor, Parrish, Copp, & Bordnick, 2011). Conceptually, the same conditioning processes can be assumed to govern the co-occurrence of a substance addiction (e.g.,
smoking) and a behavioural addiction (e.g., gambling). Indeed, evidence exists to suggest a link between substance-related
verbal cues and multi-modal gambling cues (e.g., wins, losses) (Zack, Stewart, Klein, Loba & Fragopoulos, 2005). However, research has yet to explore this relationship using discrete exteroceptive cues (i.e., cigarettes, poker chips,
cards). Thus, smoking gamblers may also develop cross-cue reactivity to simple gambling and smoking stimuli.

Aims of the present study

To date most studies examining the link between smoking and gambling have relied on self-report. We examined cross-cue reactivity
using a psychological (urges) and a physiological measure (skin conductance). We hypothesized that smoking gamblers would
show greater reactivity to smoking and gambling cues than individuals who only smoke or gamble.

As gambling preferences tend to be associated with differences in gamblers’ demographic characteristics (gender, age, education),
we sought to minimize confounding variables in this exploratory study. We recruited homogeneous community samples of regular
poker players who smoked or had never smoked, and regular smokers who had never played poker. As poker players are predominantly
male, the sample was comprised of men only.

Method

Participants

The sample consisted of 25 non-gambling smokers, 23 non-smoking gamblers (poker players) and 27 smoking gamblers (poker players),
with an average age of 27.2 years between them (range 18-61). The majority of subjects were Caucasian (85.5%), and all had
at least a high school education.

Design

We used a 3×3 mixed subjects design with cue (gambling, smoking, neutral) as the within-subjects variable and participant
(smokers, gamblers, smoking gamblers) as the between-subjects variable. Dependent variables were skin conductance, and urges
to gamble and smoke.

Skin conductance was recorded continuously during baselines and stimulus presentations with a bioamplifier (James Long Company,
Caroga Lake, NY). It employs a 500mv, 30Hz sinusoidal excitation wave form, and yields skin conductance level and response
as outputs. Ag/Ag CL electrodes and isotonic gel were attached to the distal phalanges of the non-dominant hand.

The study was approved by the university’s institutional review board, and was conducted consistent with ethical standards
laid out in the 1964 Helsinki declaration and its later amendments. After initial screening to determine frequency of smoking
and gambling, those whom we classified as regular (i.e., daily) smokers and/or poker players were invited to participate in
a study purportedly “to better understanding what people feel when they interact with a variety of stimuli.” Participants
who smoked were instructed to refrain from smoking for two hours prior to coming to the lab. Upon their arrival, participants
first provided informed consent, then completed the SOGS and FTND in counterbalanced order, followed by a CO breath reading
and the cue reactivity procedures.

After a three-minute adaptation period, participants were exposed to three sets of cues: neutral, gambling, and smoking cues.
The neutral cues were always presented first, while the order of the gambling and smoking cues was counterbalanced between
participants. To ensure standardization, participants interacted with each set for three minutes according to instructions
delivered via DVD. Before and after each cue exposure, participants relaxed for five minutes. The cues were presented on trays
covered with a cloth, and consisted of a pack of cigarettes and a lighter (smoking cues), a deck of cards and poker chips
(gambling cues), and a pack of pencils and an eraser (neutral cues). Participants were instructed to remove the cloth of a
given tray, look closely at and handle the items as they normally would (e.g., picking up a cigarette, handling the poker
cards as if dealing them, simulating writing with a pencil), then put them back on the tray, cover them, and relax. After
each cue exposure and each relaxation period, participants rated the intensity (1-10) of their urge to smoke and to gamble.
At the conclusion, participants were debriefed, received a $35 honorarium, and were entered into a raffle for a $250 prize
drawing.

Results

Urges to smoke and gamble, and of skin conductance level (SCL) after removal of one outlier, were satisfactorily distributed.
Smokers, gamblers, and smoking gamblers did not differ on any demographic variables. The impulsivity and venturesomeness subscales,
two distinct dimensions of impulsivity, were included as covariates in each analysis since impulsivity has been shown to account
for a significant portion of the variance in cue reactivity paradigms (Doran, Cook, McChargue, & Spring, 2009; Papachristou et al., 2012). For ANCOVA analyses, the adjusted means are reported unless otherwise noted.

In summary, smoking gamblers’ and pure gamblers’ urges to gamble were significantly higher (p < .001) than those of pure smokers, but did not differ in response to any of the cues (p ≥ .314). Hence this finding did not reflect cross-cue reactivity.

For smoking gamblers, urge to smoke was 6.20 (SE = 0.43) to the gambling cue, 7.45 (SE = 0.39) to the smoking cue, and 5.76 (SE = 0.41) to the neutral cue. For smokers, urge to smoke was 4.93 (SE = 0.44) to the gambling cue, 6.07 (SE = 0.40) to the smoking cue, and 4.81 (SE = 0.42) to the neutral cue. For gamblers, urge to smoke was 0.10 (SE = 0.46) to the gambling cue, 0.57 (SE = 0.42) to the smoking cue, and 0.10 (SE = 0.44) to the neutral cue.

Although smokers and smoking gamblers reported urges to smoke that were significantly higher to smoking cues than were gambling
(p ≤ .001) and neutral cues (p < .001), smoking gamblers’ urges to smoke were significantly higher (p ≤ .042) than those of pure smokers in response to both smoking and gambling cues, whereas there was no difference between
the two groups in their response to the neutral cue (p = .113). This finding supported the hypothesis of cross-cue reactivity in smoking gamblers. Pure gamblers’ urges to smoke
were significantly lower than those of smokers and smoking gamblers (p < .001), and did not differ in response to any of the cues (p ≥ .098).

To our knowledge, the present study was the first to explore cross-cue reactivity between addictive substance (nicotine) and
an addictive behaviour (gambling) using discrete cues (i.e., cigarettes, poker chips). We did not find cross-cue reactivity
for urge to gamble, but there was evidence of cross-cue reactivity between smoking and gambling cues for urge to smoke. That
is, smoking gamblers reported higher urges to smoke towards both smoking and gambling cues than did pure smokers and gamblers.
We also found that smoking gamblers overall had stronger SCL reactivity to smoking and gambling cues than did pure smokers
and gamblers. However, we also have reason to believe that the overall effect of subjective urge to smoke may have been obscured
by participants’ background urge (Ferguson & Shiffman, 2009). As smoking gamblers and smokers had abstained for several hours, their reported smoking urge to any cue was likely muddled
by internal cues of deprivation. An ad libitum smoking phase (30-60 minutes before cue exposure) might have standardized participants’
background craving (Barrett, Collins & Stewart, 2015; Carpenter et al., 2009; Traylor et al., 2011). Thus, we speculate that allowing participants to smoke one cigarette under controlled circumstances before the experimental
manipulations might in turn yield clearer evidence of cross-cue reactivity regarding urges to smoke. The results of this study
are nonetheless generally consistent with that research that has shown cross-cue reactivity involving two addictive substances.
Examples of such substances include nicotine and alcohol (Drobes, 2002; Traylor et al., 2011) or nicotine and cocaine (Taylor et al., 2000).

The smoking and gambling cues used in the present study were effective because they elicited stronger psychological and physiological
responses than did neutral cues. Consistent with our hypothesis, individuals who both smoked and gambled tended to show stronger
conditioned responses to the cues than did individuals who engaged in only one of these behaviours. Specifically, the smoking
poker players reported the highest urges to smoke (although their urges to gamble did not surpass those of the pure poker
players). The smoking poker players also described larger physiological reactivity in SCL in response to all cues, as compared
to pure smokers or pure gamblers. These findings are consistent with the hypothesis that cross-cue reactivity is enhanced
via classical conditioning, and that dually addicted individuals may experience the largest increases in sympathetic nervous
system activity. Furthermore, the increase in subjective and physiological arousal resulting from dual addiction can be explained
by one or more psychobiological models of craving (for review, see Skinner & Aubin, 2010). For instance, considering the incentive sensitization model (Robinson & Berridge, 1993), one might conclude that concomitant substance use and gambling results in more frequent or pervasive activation of neural
systems than either activity alone, and that this “dual activation” might result in greater sensitization of neural systems,
more pronounced sensitization-related neuroadaptation in these systems and an overall increase in the incentive salience of
cues. However, the neurobiological effects of a dual substance and behavioural addiction are unknown, thereby warranting further
investigation.

The finding that smoking poker players did not report stronger urges to gamble than pure poker players was somewhat unexpected.
The most likely explanation is that the smoking poker players in this community sample were similar in gambling severity to
their non-smoking counterparts. Based on SOGS scores, many subjects were classified as social gamblers, i.e., they were not
“addicted” to gambling. We speculate that the results might have been different if we had recruited pathological or treatment-seeking
gamblers, such as those of Petry and Oncken (2002) or Potenza et al. (2004). Such a difference would be consistent with recent findings that daily tobacco-using gamblers in treatment have significantly
greater gambling severity and also more severe comorbidity (McGrath & Barratt, 2009; Odlaug et al., 2012). Therefore, cigarette-smoking pathological gamblers might well experience stronger urges to gamble compared to their non-smoking
counterparts. On the other hand, there is also evidence that smoking gamblers are not a homogeneous group: apparently a subset
of gamblers who smoke find that smoking lessens their urges to gamble, even though others consider smoking urge-inducing (Odlaug et al., 2012). These findings indicate that more research is needed to shed further light on these important questions.

While this study provides some evidence that gambling cues can become conditioned stimuli (CSs) for urges to smoke, the inverse
was not also observed—i.e., with smoking gamblers, the smoking cues did not, in fact, elicit strong urges to gamble. A possible
explanation for this finding is extinction or even conditioned inhibition (Bouton, 2007). These phenomena lead to a decrease in the response to a CS when that stimulus is regularly presented without the US following
acquisition (i.e., CS-US pairings). For example, smoking poker players are likely to encounter smoking stimuli frequently,
in their daily lives, in multiple venues outside of gambling; these presentations of CSs without the US may either extinguish
or inhibit smokers’ gambling urge in response to smoking stimuli. The opposite is true of poker stimuli because they are typically
not present outside of a gaming environment. Moreover, smoking poker players are likely to smoke each and every time they
gamble. Gambling cues are thus rarely present in the absence of nicotine ingestion. We therefore speculate that, under these
circumstances, gambling stimuli will be better at acquiring CS properties for smoking than vice versa.

Limitations

Several limitations should be noted. First, as mentioned, participants were merely exposed to, and interacted minimally with,
gambling and smoking stimuli. Although this is common in cue-reactivity research with smokers, gambling cue-reactivity research, in contrast, has often tried to mimic the real-world gambling environment more closely by allowing
participants to gamble and wager small amounts of money. The method used in the present study may have prevented much of the
excitement people typically experience when gambling because, in such circumstances, they can win money. Therefore, replicating
the study with a preparation that involves actual gambling should be considered to obtain more meaningful physiological and
subjective measures of urge under more arousing circumstances. One might also consider using multidimensional measures of
urge in addition to subjective ratings based on Likert-scale measurements.

A second limitation is that for the reasons previously explained we only enrolled men in this study and do not know whether
the findings hold true for both sexes. A replication of cross-cue reactivity involving a substance and a behavioural addiction
that includes women is indicated. Similarly, the current findings are limited to poker players. We chose them for this study
because of the frequent comorbidity of nicotine dependency and problem gambling in card players. But future studies should
seek to replicate the results with gamblers who prefer other gambling modalities in which cue-elicited arousal plays a central
role (e.g., electronic gaming machines).

Finally, as indicated above, the participants in this study were indeed regular smokers and gamblers, but on average did not
also show a clinically significant, pathological involvement with gambling. Cross-cue reactivity may be more pronounced in
nicotine-dependent pathological gamblers, and future studies should be conducted with treatment-seeking smokers and gamblers.

Conclusions

Despite limitations, the present findings provide initial support for a cross-cue reactivity model as it applies to smoking
poker players. Compared to pure smokers or gamblers, these individuals showed overall stronger physiological arousal (SCL)
and stronger urges to smoke, although their urges to gamble did not surpass the urges of pure gamblers. If the present findings
are replicated with treatment-seeking samples, the way treatment is administered to dually addicted individuals may change
accordingly. Because of cross-cue reactivity and smoking gamblers’ overall higher physiological arousal (as measured by SCL),
we surmise that dually addicted individuals probably experience more frequent and possibly stronger urges to engage in the
addictive behaviours. If a heavy gambler attempted to abstain from smoking, exposure to gambling cues might precipitate relapse,
because the gambling cues will elicit urges to smoke. The same reasoning applies to smokers who seek to refrain from gambling,
but do not also quit smoking. Interventions may have to be geared towards simultaneously treating smoking and gambling problems.

We know from treatment outcome research that cigarette-smoking alcohol abusers who quit smoking were more likely to maintain
the alcohol-related treatment gains than those who did not (Bobo, McIlvain, Lando, Walker, & Leed-Kelly, 1998). Analogously, the addition of a smoking-cessation component to gambling treatment, and vice versa, may lead to better outcomes
for dually addicted individuals than treating either problem in isolation. Therapists are therefore encouraged to assess the
potential benefits of interventions that target both behaviours in cross-addicted individuals.